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THE QUALITY OF TRABECULAR BONE ASSESSED USING

CONE-BEAM COMPUTED TOMOGRAPHY

O.T. DAVID, M. LERETTER, A. NEAGU#

“Victor Babeş” University of Medicine and Pharmacy, Timişoara, 2, Eftimie Murgu sq., 300041
Timişoara, Romania; #e-mail: neagu@umft.ro

Abstract. Dental implant stability depends on the quality of bone in the target site. Although
subjective bone quality assessments are still important, objective measurements of bone density by X-
ray imaging is increasingly appreciated in implant planning. Using conventional computed
tomography (CT), an objective bone density scale was established in terms of mean CT numbers of
various bone types, which characterize their ability to attenuate X-ray beams. Cone-beam computed
tomography (CBCT) is preferred for three-dimensional dental imaging because it is cheaper than CT
and exposes the patient to lower doses of X-rays. The results of bone density measurements by
CBCT, however, are less consistent than CT results: they depend on the type of CBCT device and on
image acquisition parameters. Here we analyzed CBCT images of 46 patients, recorded in identical
conditions by the same type of CBCT unit. We computed the CT numbers of cancellous bone from
400 potential implant sites. Moreover, for each site, we recorded the standard deviation of the CT
numbers of constituent voxels, which is a measure of bone heterogeneity. We classified the sites in
eight groups, according to gender and location (anterior and posterior regions of the mandible and the
maxilla). Based on the one-way ANOVA test and on the Kruskal-Wallis test, we found that
significant differences exist between the mean values of CT numbers and the standard deviations of
CT numbers. Our study suggests that, under identical conditions, CBCT is able to detect differences
in bone density and microstructure. The CBCT scale established here for trabecular bone density and
heterogeneity might be useful for pre-operative evaluation of bone quality.
Key words: CT number, radiodensity, Hounsfield unit (HU), dental implant.

INTRODUCTION

To withstand masticatory forces, a dental implant needs to transmit loads via


the bone-to-implant interface. Therefore, the success of oral implantology hinges
on a correct assessment of bone quality in the receiving site. The bone density scale
proposed by Misch [14], although subjective, proved useful in this respect,
allowing for pre-operative assessment of the load bearing capacity of the bone from
the target site. Misch classified bones of the dental arches in five bone density
_______________________
Received: January 2015
in final form: January 2015

ROMANIAN J. BIOPHYS., Vol. 24, No. 4, P. 227–241, BUCHAREST, 2014


228 O.T. David, M. Leretter, A. Neagu 2

classes, ranging from D1 to D5: D1 bone is dense cortical bone, D2 bone is thick
dense-to-porous cortical bone that wraps a coarse trabecular bone, D3 bone is thin
porous cortical bone that wraps a fine trabecular bone, D4 is fine trabecular bone
within the ridge and minimal or no cortical bone on the crest, whereas D5 is
immature, non-mineralized bone [14, 15].
The quality of bone depends on the anatomical location. The most dense bone
type is found in the anterior mandible, being followed by the posterior mandible,
the anterior maxilla, and the posterior maxilla. The anterior mandible is mainly
composed of D2 bone, but also contains D1 bone in about 6% of the population;
the posterior mandible is made of D2 bone and D3 bone, and rarely contains D1
bone and D4 bone; the anterior maxilla is mainly made of D3 bone, but also of D2
bone (25% occurrence) and D4 bone (10% occurrence); the posterior maxilla is
made of D3 bone and D4 bone, and, occasionally, of D2 bone (10% occurrence)
[15].
An important leap in bone quality estimation was made using computed
tomography (CT), by characterizing bone density in terms of the CT number (or
radiodensity), expressed in Hounsfield units (HU) [18]. The CT number describes
the ability of a substance to attenuate an X-ray beam, ranging from –1000 HU for
air to about 3000 HU for enamel [9]. A significant correlation was found between
the observed radiodensities of the implant sites and their subjective bone density
scores [18]. Further studies [12, 20, 23, 24] have established the ranges of HU
values corresponding to each bone density class: D1 bone > 1250 HU, D2 bone
850–1250 HU, D3 bone 350–850 HU, D4 bone 150–350 HU and D5 bone < 150
HU [15].
Nevertheless, for the three-dimensional (3D) visualization of hard tissues
from the oral environment CT is not the imaging technique of choice; it exposes
the patient to relatively high doses of ionizing radiation and requires expensive
equipment. Instead, cone beam computed tomography (CBCT) is preferred because
it involves less radiation exposure (by about one order of magnitude) and requires a
device that is about five times cheaper than a full-body CT scanner [7, 22]. While
in a conventional CT scanner the body part of interest is traversed by a fan-shaped
beam of X-rays that falls on a linear arrangement of detectors, in a CBCT device
the investigated body part is traversed by a cone-shaped beam of X-rays that falls
on a flat panel detector (such as a screen of scintillator crystals placed on a matrix
of photodiodes embedded in solid-state amorphous silicon; the scintillator crystals
convert X-rays into visible light, which is detected by the photodiodes) [13].
CBCT is routinely used to visualize the bony structures of the head and neck
with typical voxel sizes as small as 0.2×0.2×0.2 mm. The image reconstruction
software associates to each voxel a HU value, also called CT number in the
literature, although it is recorded using a CBCT device. Commercially available
3 Trabecular bone assessed using CBCT 229

CBCT systems, however, have a contrast resolution of approximately 10 HU,


whereas state-of-the-art multi-detector helical CT scanners have contrast
resolutions of the order of 1 HU. This discrepancy originates from the different
beam geometry (the cone beam favors X-ray scattering) and from differences in
detector performance [13]. A CBCT device is calibrated by the manufacturer to
give –1000 HU for air and 0 HU for a water phantom, but daily calibrations of the
detector and the X-ray tube, as usual for CT scanners, are not carried out for CBCT
units. Therefore, CT numbers in CBCT are not absolute values [17].
When CBCT was used to assess bone density, the results were found to
depend on the type of device, on the image acquisition parameters, and on the
position of the evaluated tissue with respect to the field of view [16, 19]. Therefore,
the use of CBCT for bone density evaluation is a subject of intense research [1, 2,
3, 4, 10, 21].
In this work we focus on CBCT assessment of the quality of trabecular bone
from the mandible and the maxilla. We concentrate on the trabecular bone because
it is the most homogeneous part of the hard tissue from an implant site, and it has
been carefully characterized in terms of HU values measured using conventional
CT [6]. Thus, our results can be compared with a reliable set of reference values.
For consistency, we analyze data recorded with a single type of CBCT
device, using the same image acquisition parameters (tube voltage, current
intensity, voxel size and field of view). In this way we minimize the number of
factors that are known to affect the bone density estimation by CBCT [16].
Besides the mean CT numbers of the bone samples, we also analyze the
standard deviations of the CT numbers of the constituent voxels. Each voxel is
characterized by a CT number (voxel value), and the CBCT image analysis
software reports both the mean value and the standard deviation of CT numbers of
the voxels that belong to the selected volume. The latter is a measure of bone
heterogeneity. Coarse trabecular bone is more heterogeneous than fine trabecular
bone, so we hypothesize that the standard deviations of HU values obtained by
CBCT might reveal differences between different types of cancellous bone.
Our study also deals with the gender dependence of the trabecular bone
density. To this end, we analyze the same number of sites for men and women.
Nevertheless, in this work we do not take into account certain factors that
might impact bone density, such as age, medication, nutritional status, and lifestyle.
The main question we address here is whether there are significant
differences between the mean CT numbers and the standard deviations of CT
numbers of trabecular bones from different regions of the dental arches. If so, it
would prove that, under similar settings, CBCT is capable to distinguish
differences in bone quality, allowing one to establish quantitative criteria for bone
density assessment by CBCT.
230 O.T. David, M. Leretter, A. Neagu 4

MATERIALS AND METHODS

PATIENTS

For this retrospective study 46 edentulous patients were selected from the
Mall Dental Clinic Timisoara, Romania, who had undergone a CBCT investigation,
between 2011 and 2013, for reasons that had nothing to do with the present study.
No patient was subject to ionizing radiations for the sake of this work.
To enroll patients, we relied on the following inclusion criteria: (i) CBCT
images were recorded using a tube voltage of 84 kV and a current intensity of
14 mA, (ii) the CBCT images were recorded with a cylindrical field of view (FOV)
of 80 mm both in diameter and height (Figure 1), (iii) the voxel size was
0.2×0.2×0.2 mm, (iv) the dental arches were positioned similarly in the FOV, as
depicted in Figure 1.

Coronal Sagittal

Axial

Fig. 1. The field of view (FOV) was a cylinder of 80 mm in diameter


and height. The lower right panel is a 3D rendering of a full-scull
CBCT image, whereas the other panels represent cross-sections of the
same image, taken in the axial, coronal and sagittal plane.

We excluded from the study patients who had pathologic and/or traumatic
lesions of the jaws.
To assure gender balance, an equal number of men and women were enrolled
in the study. Moreover, the number of investigated implant sites was the same for
each gender.
5 Trabecular bone assessed using CBCT 231

Once we identified eligible patients, we contacted them, explained the details


of this retrospective study in what concerns the handling of their data, and asked
them to sign a form of informed consent.

IMAGE ACQUISITION AND BONE DENSITY ASSESSMENT

For image acquisition, we used a ProMax 3D CBCT unit (Planmeca,


Finland), with settings specified in the previous section. Images were saved in
DICOM format. To locate implant target sites and to record the mean CT number
of the trabecular bone from these sites, we used the Romexis 3.0.1.R software
(Planmeca, Finland). In each site, our region of interest was a rectangular volume
of trabecular bone located within the alveolar ridge (Figure 2).

Fig. 2. A typical CBCT recording included in this study, taken with the
cylindrical field of view highlighted in Figure 1. The region of interest is a
rectangular slab of trabecular bone located in edentulous regions of the
alveolar ridge. The Romexis software characterizes the selected volume
(white text in frame), listing its size, the mean value of the CT numbers
associated to the voxels that compose it (labeled as “Mediu”), the standard
deviation of the CT numbers of the constituent voxels (labeled as “Deviaţie
std”), and the range of CT numbers of the voxels from the volume (listed in
the format R [smallest CT number, largest CT number]).
232 O.T. David, M. Leretter, A. Neagu 6

Each voxel of this volume is characterized by a CT number, expressed in HU.


The software displays the mean value of the CT numbers of the constituent voxels,
the standard deviation of these CT numbers, as well as the range of HU values (the
smallest and the largest HU values encountered in the volume) (Figure 2).

STATISTICAL ANALYSIS

We divided the trabecular bone samples into eight groups according to


gender and anatomical location: 1 – women anterior maxilla, 2 – women posterior
maxilla, 3 – women anterior mandible, 4 – women posterior mandible, 5 – men
anterior maxilla, 6 – men posterior maxilla, 7 – men anterior mandible, 8 – men
posterior mandible. In each dental arch, anterior and posterior regions were
delimited by the mesial surface of the first premolar.
To test whether there are significant differences between the mean values
obtained for the 8 groups, we performed a one-way analysis of variance (one-way
ANOVA) and a Kruskal-Wallis test [5] using the Statistics Toolbox from
MATLAB 7.13 (MathWorks, Natick, MA, USA). These tests reveal whether the
mean values of all groups are equal or not, but they do not tell which pairs of
means differ significantly from each other. To address this problem, we used the
honestly significant difference (Tukey-Kramer) criterion to perform multiple
comparisons between means.
Since ANOVA relies on the assumption that the data are normally distributed
[5], we applied the Jarque-Bera test to accept or reject the null hypothesis that the
data from each group come from a normal distribution.

RESULTS

According to the inclusion criteria, our study was conducted on CBCT


recordings of 23 men and 23 women. A total of 400 volumes (sites) of trabecular
bone were sampled from edentulous regions of the alveolar bone; these sites were
divided into eight groups, as described in the previous section. Table 1 presents the
descriptive statistics of the mean CT numbers of the trabecular bones from each
group.
To test whether the data are normally distributed, we performed a Jarque-
Bera test, which is a two-sided goodness-of-fit test suitable to decide whether the
null hypothesis (H0: the data are normally distributed with unspecified mean and
standard deviation) or the alternative hypothesis (Ha: the data are not normally
distributed) is valid. The last column of Table 1 lists the corresponding P-values
for a significance level of 5%. Small values of P cast doubt on the validity of H0.
7 Trabecular bone assessed using CBCT 233

Table 1
Descriptive statistics of the CT numbers of the investigated trabecular bone volumes. The last column
lists the P-values of the normality test
Gender Anatomical Number of Mean CT Standard Skewness Kurtosis P
location sites number error
(HU) (HU)
Anterior maxilla 34 354 30.0 0.3235 3.401 > 0.5
Posterior maxilla 66 193 17.4 0.6999 2.828 0.046
Women
Anterior mandible 27 514 30.5 0.4455 2.086 0.185
Posterior mandible 73 234 17.5 0.9581 3.369 0.012
Anterior maxilla 40 473 33.5 –0.1010 3.289 > 0.5
Posterior maxilla 60 250 18.7 0.8194 3.277 0.031
Men
Anterior mandible 28 521 22.0 0.7559 3.806 0.071
Posterior mandible 72 389 28.0 0.6159 2.689 0.057

We also analyzed the standard deviations of the CT numbers of the voxels


that compose the 3D image of the regions of interest; the results of their descriptive
statistics are listed in Table 2, along with the P-values of the Jarque-Bera test of
normality (last column).

Table 2
Descriptive statistics of the standard deviations (SD) of CT numbers of voxels that compose the
image of the trabecular bone of interest. The last column lists the P-values of the normality test
Gender Anatomical Number of Mean SD of Standard Skewness Kurtosis P
location sites CT numbers error
(HU) (HU)
Anterior maxilla 34 206 7.57 –0.165 2.544 > 0.5
Posterior maxilla 66 176 5.08 0.4987 2.765 0.133
Women
Anterior mandible 27 243 10.1 0.0904 2.539 > 0.5
Posterior mandible 73 212 5.13 0.2695 2.282 0.184
Anterior maxilla 40 208 5.67 –0.1041 2.159 0.389
Posterior maxilla 60 193 4.66 0.2782 2.224 0.193
Men
Anterior mandible 28 247 11.3 0.07911 2.495 > 0.5
Posterior mandible 72 220 5.44 0.4889 3.284 0.120

To test whether there are significant differences between the mean CT


numbers obtained for the eight groups of trabecular bone volumes, we performed a
one-way ANOVA test, which tells whether to accept the null hypothesis (H0: the
mean values of CT numbers are equal) or the alternative hypothesis (Ha: not all the
means are equal).
Using the anova1 function from MATLAB's Statistics Toolbox, we generated
box plots (Figure 3), which characterize the eight groups of trabecular bone slabs.
In the left panel, on each box, the central line is the median of the CT numbers
obtained for the bone regions that belong to the respective group. The edges of the
box mark the first and the third quartile (that is, half of the data points lie within the
234 O.T. David, M. Leretter, A. Neagu 8

box), whereas the whiskers span the interval between extreme data points not
classified as outliers. Individual markers (+ signs) represent outliers. The right
panel represents similar box plots of the standard deviations of CT numbers of the
constituent voxels.

Fig. 3. Box plots of the medians of the CT numbers (left) and the medians of the standard deviations of CT
numbers (right) obtained for eight groups of trabecular bone volumes: 1 – women anterior maxilla,
2 – women posterior maxilla, 3 – women anterior mandible, 4 – women posterior mandible, 5 – men
anterior maxilla, 6 – men posterior maxilla, 7 – men anterior mandible, 8 – men posterior mandible.

Table 3 presents the results of this test as a standard one-way ANOVA table
[5]. In the terminology of ANOVA distinct groups are called treatments. The first
row of Table 3 refers to treatments: 7 is the number of degrees of freedom (equal to
the number of treatments minus 1), the number listed in the next column (SS) is the
treatment sum of squares, it is followed by the treatment mean square (in column
MS), by the F-statistic given by the ratio of the variation among sample means to
the variation within the samples (column F), and the corresponding P-value. The
second row of Table 2 refers to errors: the number of degrees of freedom is the
number of observations minus the number of treatments (column df); it is followed
by the error sum of squares (column SS), and the error mean square (column MS,
given by the ratio of the error sum of squares to the number of degrees of freedom
for errors).

Table 3
The results of the one-way ANOVA test for the mean CT numbers of the voxels that compose the
trabecular bone volumes under study
Source df SS MS F P
Groups 7 5.3284×106 7.6120×105 25.03 3.2168×10–28
Error 392 1.1922×107 3.0413×104 – –
Total 399 1.7250×107 – – –

The large value of F suggests that the discrepancies between sample means
might not stem from discrepancies between the values that belong to individual
9 Trabecular bone assessed using CBCT 235

samples. Can we conclude that there are significant differences between the
means? In a hypothesis test, the decision is based on the P-value, which is the
probability of obtaining the observed results when H0 is true. The small value of P,
(more precisely, P < 0.05 at a 5% significance level) indicates that H0 can be
rejected in favor of Ha; that is there are significant differences between certain
mean values.
One-way ANOVA was also used to test whether there are significant
differences between the mean values of the standard deviations of CT numbers of
the voxels that compose the 3D images of the bone slabs under study. Table 4 lists
the results of this test, indicating that not all means are equal.

Table 4
The results of the one-way ANOVA test for the mean values of the standard deviations of CT
numbers of the voxels that compose the investigated trabecular bone volumes
Source df SS MS F P
Groups 7 1.6811×105 2.4016×104 12.41 2.2605×10–14
Error 392 7.5872×105 1.9355×103 – –
Total 399 9.2683×105 – – –

The one-way ANOVA tests presented in Tables 3 and 4 reveal significant


differences between means.

Table 5
The results of the Kruskal-Wallis test for the mean CT numbers of the voxels from trabecular bone
samples
Source df SS MS Chi-sq P
Groups 7 1.7695×106 2.5279×105 132.39 1.9938×10–25
Error 392 3.5637×106 9.0910×103 – –
Total 399 5.3332×106 – – –

Table 6
The results of the Kruskal-Wallis test for the mean values of the standard deviations of CT numbers
of the voxels from trabecular bone samples
Source df SS MS Chi-sq P
Groups 7 8.6215×105 1.2316×105 64.51 1.8902×10–11
Error 392 4.4706×106 1.1405×104 – –
Total 399 5.3328×106 – – –

Since the ANOVA test is based on the assumption that the data are normally
distributed [5], and the normality test gave a borderline result for groups 2, 4, 6 and
8 (see last column of Table 1, values corresponding to posterior regions of the
dental arches), we also performed a Kruskal-Wallis test for the same null
hypothesis (H0) and alternative hypothesis (Ha). Tables 5 and 6 show the results of
236 O.T. David, M. Leretter, A. Neagu 10

the Kruskal-Wallis test for the mean CT numbers and the mean values of the
standard deviations of CT numbers, respectively.
Hence, both the one-way ANOVA test and the Kruskal-Wallis test indicate
that not all means are equal. These tests, however, do not give any hint on which
pairs of means differ from each other. To address this question, we performed
multiple comparisons using the multcompare function from the Statistics Toolbox
of MATLAB. The results of multiple comparisons are shown on Figure 4.

Fig. 4. Multiple comparisons of the mean values of CT numbers (A) and standard
deviations of CT numbers (B) based on the one-way ANOVA test; multiple
comparisons of the mean ranks of CT numbers (C) and mean ranks of standard
deviations of CT numbers (D) based on the Kruskal-Wallis test. The groups of
trabecular bone regions under study are: 1 – women anterior maxilla, 2 – women
posterior maxilla, 3 – women anterior mandible, 4 – women posterior mandible,
5 – men anterior maxilla, 6 – men posterior maxilla, 7 – men anterior mandible,
8 – men posterior mandible.

Figure 4A refers to the mean CT numbers of the eight populations (groups of


trabecular bone slabs) under study. Circular markers represent the mean values and
horizontal lines span their intervals of confidence, calculated at the 95% level of
confidence. Two means differ significantly if their intervals of confidence do not
overlap. For example, to identify the groups whose mean CT numbers differ from
the mean CT number of group 3, it is useful to draw two vertical lines at the
11 Trabecular bone assessed using CBCT 237

extremities of the corresponding confidence interval (dotted lines on Figure 4A);


the means that differ from the mean of group 3 are the ones whose confidence
interval plots do not extend in the area delimited by the vertical lines. Thus, we
conclude that the mean CT numbers of groups 1, 2, 4, 6, and 8 differ significantly
from the mean CT number of group 3. The Kruskal-Wallis result shown on Figure
4C can be analyzed in a similar fashion.
The analysis of Figures 4B and 4D allows one to identify groups for which
the mean values of standard deviations of CT numbers differ significantly from the
mean of a selected group. For example, the dotted vertical lines drawn on the
multiple comparison plot of Figure 4B show that, regarding the standard deviations
of CT numbers, the mean of group 7 differs significantly from the means of groups
1, 2, 4, 5, and 6.

DISCUSSION

An important problem in dental implant planning is the evaluation of bone


quality in prospective implant sites. CT numbers recorded with fan-beam CT
devices represent an objective scale for bone density, which strongly correlates
with subjective bone quality scores. Moreover, mean CT numbers of implant sites
strongly correlate also with their anatomical location [18]. Recording the mean CT
numbers of 139 implant sites, Norton and Gamble reported that the average values
of CT numbers were 970 HU for the anterior mandible, 696 HU for the anterior
maxilla, 669 HU for the posterior mandible, and 417 HU for the posterior maxilla
[18]. This hierarchy of the mean bone densities of the four jaw regions, seen also in
the present work, has been observed in several studies [6, 11, 23, 24].
To characterize trabecular bone density in terms of HU, de Oliveira et al.
have examined CT recordings of 75 potential implant sites, obtaining mean voxel
values of 383 HU for the anterior mandible, 370 HU for the anterior maxilla, 306
HU for the posterior mandible and 256 HU for the posterior maxilla [6]. Typical
ranges of HU values were established as follows: poor quality, fine trabecular bone
(the cancellous component of D4 or D5 bone) had CT numbers lower than 200,
whereas high quality, coarse trabecular bone had CT numbers higher than 400; the
interval between these limits corresponds to intermediate quality trabecular bone
[6]. Although measured using a CBCT device, our results fall within these ranges,
with standard errors of less than 10% of the mean (Table 1). One notable exception
is the mean radiodensity of cancellous bone from the posterior maxilla of men
(about 250 HU). Nevertheless, this value lies within the HU range for D4 bone,
which mainly consists of fine trabecular bone [15].
The mean values of CT numbers obtained in our study (Table 1) are also
comparable with the ones inferred by Fuh et al. from CT scans of 35 women and
27 men, with a total of 154 potential implant sites analyzed: the trabecular bone
238 O.T. David, M. Leretter, A. Neagu 12

density was found to be the highest in the anterior mandible (530 HU), followed by
the anterior maxilla (516 HU), the posterior mandible (359 HU) and the posterior
maxilla (332 HU) [8]. In what concerns the anterior mandible our results are closer
to the ones of ref. [8], whereas for the posterior maxilla our results are closer to the
ones of ref. [6].
In their study of trabecular bone from the mandible by CBCT and multislice
helical CT [17], Naitoh et al. found a strong correlation between voxel values (HU
values) measured via CBCT and bone mineral density obtained by helical CT.
Nevertheless, their CBCT-derived voxel values, of 655 HU to 747 HU for the
anterior mandible, and 519 HU for the posterior mandible, are higher than ours,
although their study group consisted mainly of women (4 men and 12 women).
This discrepancy might stem from using a different type of CBCT unit, Alphard
VEGA (Asahi Roentgen Ind. Co., Japan), and different settings [17].
Bone density measurements in HU units were performed on 236 potential
implant sites identified in CBCT scans of 74 men and 54 women, recorded by the
same type of unit as ours, at slightly different settings (90 kV, 14 mA, and voxel
size of 0.2×0.2×0.2 mm) [10]. Although it does not focus on trabecular bone, but
on bone located in the vicinity of a cylindrical implant simulated using the
Simplant software, a comparison with our results is justified for D4 bone, which is
basically cancellous. Moreover, it is reasonable to assume that the simulated
implants, 4.1 mm in diameter and 10 mm in length, placed in edentulous spans of
the posterior jaws are mainly surrounded by trabecular bone. Indeed, the mean CT
numbers of the posterior mandible (394 HU) and the posterior maxilla (220 HU)
are comparable with our results. The slightly higher HU value observed by Hao et
al. in the posterior mandible and the significantly higher HU values observed in the
anterior jaws might stem from cortical bone contributions [10].
Significant differences between means can be identified from Figure 4
keeping in mind that the Kruskal-Wallis test is less efficient than the one-way
ANOVA test when the assumptions for applying the latter hold [5]. Thus, for
analyzing HU values, for which the normality test gave borderline results, the
Kruskal-Wallis test is more reliable. This was the statistical test of choice also in
reference [8] for the analysis of CT numbers of trabecular bone acquired by
conventional CT. In our study, according to the last column of Table 1, HU values
of samples from the anterior portion of the dental arches are normally distributed,
while the HU values of samples from the posterior regions are not (excepting the
posterior mandible of men, whose P-value, however, barely exceeds 0.05).
Therefore, to identify mean HU values that differ significantly from each other, it
is preferable to rely on the confidence intervals of mean ranks shown in Figure 4C,
derived from multiple comparisons based on the Kruskal-Wallis test (instead of
Figure 4A, which stem from the one-way ANOVA test). For instance, looking at
the region delimited by the dotted lines from Figure 4C, we infer that the mean CT
number of group 1 (anterior maxilla of women) differs significantly from the mean
13 Trabecular bone assessed using CBCT 239

CT numbers of groups 2, 4 and 7. The same figure shows that the mean CT number
of trabecular bone from the anterior mandible of men (521 HU) is significantly
higher than the mean CT numbers of other groups, except for the anterior mandible
of women (514 HU) and anterior maxilla of men (473 HU). Moreover, we remark
that, for each anatomical region, the mean CT number is larger for men than for
women, but their difference is not significant from the statistical point of view.
For analyzing standard deviations of HU values (which are normally
distributed according to Table 2) multiple comparisons based on the one-way
ANOVA test (Figure 4B) are more powerful than those based on the Kruskal-
Wallis test (Figure 4D) [5]. From the dotted lines of Figure 4B we infer that,
regarding standard deviations of CT numbers of the constituent voxels, the mean of
group 7 (anterior mandible of men) is significantly larger than the means of other
groups, except for groups 3 (anterior mandible of women) and 8 (posterior
mandible of men). Thus, standard deviations of CT numbers of the constituent
voxels discriminate between coarse and fine trabecular bone. Just as in the case of
mean voxel values, for each anatomical region, the standard deviation of CT
numbers is larger for men than for women, but not significantly so from the
statistical point of view.

CONCLUSIONS

In this article we have analyzed voxel values of trabecular bone samples, as a


function of gender and anatomical location, measured by one type of CBCT unit,
ProMax 3D (Planmeca, Finland), under identical conditions.
The Kruskal-Wallis test applied for the mean values of CT numbers revealed
that not all means are equal, and multiple comparisons have identified the groups
whose means differ significantly from each other.
Due to the normal distribution of the data, the one-way ANOVA test was
suitable for pointing out significant differences between mean values of the
standard deviations of CT numbers of voxels that compose the investigated bone
slabs. These standard deviations are a measure of structural heterogeneity, and their
analysis suggests that CBCT detects significant differences between fine and
coarse trabecular bone. Since the software provided by manufacturers of CBCT
units routinely report these standard deviations, the methodology presented here is
within the reach of implant specialists for pre-operative assessment of the
coarseness of trabecular bone.
By identifying conditions of systematic bone density analysis, and
establishing mean values of CT numbers and standard deviations of CT numbers as
a function of gender and anatomical location, our study might help clinicians using
the same type of CBCT unit in evaluating the quality of trabecular bone from
prospective implant sites.
240 O.T. David, M. Leretter, A. Neagu 14

Acknowledgements. This paper was published under the frame of the European Social Fund,
Human Resources Development Operational Programme 2007–2013, project No.
POSDRU/159/1.5/136893.

REFERENCES

1. ANGELOPOULOS, C., W.C. SCARFE, A.G. FARMAN, A comparison of maxillofacial CBCT


and medical CT, Atlas of the oral and maxillofacial surgery clinics of North America, 2012, 20,
1–17.
2. AZEREDO, F., L.M. DE MENEZES, R. ENCISO, A. WEISSHEIMER, R.B. DE OLIVEIRA,
Computed gray levels in multislice and cone-beam computed tomography, American Journal of
Orthodontics and Dentofacial Orthopedics, 2013, 144, 147–155.
3. CARRAFIELLO, G., M. DIZONNO, V. COLLI, S. STROCCHI, S. POZZI TAUBERT, A.
LEONARDI, et al., Comparative study of jaws with multislice computed tomography and cone-
beam computed tomography, Radiol. Med., 2010, 115, 600–611.
4. CASSETTA, M., L.V. STEFANELLI, A. PACIFICI, L. PACIFICI, E. BARBATO, How
accurate is CBCT in measuring bone density? A comparative CBCT-CT in vitro study. Clinical
Implant Dentistry and Related Research, 2014, 16, 471–478.
5. DALGAARD, P., Introductory Statistics with R, Second Edition, Springer Science+Business
Media, LLC, New York, 2008.
6. DE OLIVEIRA, R.C.G., C.R. LELES, L.M. NORMANHA, C. LINDH, R.F. RIBEIRO-
ROTTA, Assessments of trabecular bone density at implant sites on CT images. Oral Surgery
Oral Medicine Oral Pathology Oral Radiology and Endodontology, 2008, 105, 231–238.
7. DE VOS, W., J. CASSELMAN, G.R.J. SWENNEN, Cone-beam computerized tomography
(CBCT) imaging of the oral and maxillofacial region: A systematic review of the literature,
International Journal of Oral and Maxillofacial Surgery, 2009, 38, 609–625.
8. FUH, L.J., H.L. HUANG, C.S. CHEN, K.L. FU, Y.W. SHEN, M.G. TU, W.C. SHEN, J.T. HSU,
Variations in bone density at dental implant sites in different regions of the jawbone, J. Oral.
Rehabil., 2010, 37, 346–351.
9. GULSAHI A, Bone quality assessment for dental implants. In: I. Turkyilmaz (ed.) Implant
Dentistry – The Most Promising Discipline of Dentistry, InTech, Rijeka, 2011, Ch. 20,
pp. 437–452.
10. HAO, Y., W. ZHAO, Y. WANG, J. YU, D. ZOU, Assessments of jaw bone density at implant
sites using 3D cone-beam computed tomography, Eur. Rev. Med. Pharmacol. Sci., 2014, 18,
1398–1403.
11. HIASA, K., Y. ABE, Y. OKAZAKI, K. NOGAMI, W. MIZUMACHI, Y. AKAGAWA,
Preoperative computed tomography-derived bone densities in hounsfield units at implant sites
acquired primary stability. ISRN Dentistry, 2011, 678729.
12. KOBAYASHI, F., J. ITO, T. HAYASHI, T. MAEDA, A study of volumetric visualization and
quantitative evaluation of bone trabeculae in helical CT: Quantitative evaluation of bone
trabeculae, Dentomaxillofacial Radiology, 2003, 32, 181–185.
13. MIRACLE, A.C., S.K. MUKHERJI, Conebeam CT of the head and neck, Part 1: Physical
principles, American Journal of Neuroradiology, 2009, 30, 1088–1095.
14. MISCH, C.E., Density of bone: effect on treatment plans, surgical approach, healing, and
progressive bone loading. The International Journal of Oral Implantology: Implantologist, 1990,
6, 23–31.
15. MISCH, C.E., Contemporary Implant Dentistry, Third Edition, Mosby Inc., St. Louis, 2008.
16. NACKAERTS, O., F. MAES, H. YAN, P. COUTO SOUZA, R. PAUWELS, R. JACOBS,
Analysis of intensity variability in multislice and cone beam computed tomography. Clinical
Oral Implants Research, 2011, 22, 873–879.
15 Trabecular bone assessed using CBCT 241

17. NAITOH, M., A. HIRUKAWA, A. KATSUMATA, E. ARIJI, Evaluation of voxel values in


mandibular cancellous bone: relationship between cone-beam computed tomography and
multislice helical computed tomography, Clinical Oral Implants Research, 2009, 20, 503–506.
18. NORTON, M.R., C. GAMBLE, Bone classification: an objective scale of bone density using the
computerized tomography scan, Clinical Oral Implants Research, 2001, 12, 79–84.
19. OLIVEIRA, M.L., G.M. TOSONI, D.H. LINDSEY, K. MENDOZA, S. TETRADIS, S.M.
MALLYA, Influence of anatomical location on CT numbers in cone beam computed
tomography, Oral Surg. Oral Med. Oral Pathol. Oral Radiol., 2013, 115, 558–564.
20. PARK, H.-S., Y.-J. LEE, S.-H. JEONG, T.-G. KWON, Density of the alveolar and basal bones
of the maxilla and the mandible, American Journal of Orthodontics and Dentofacial
Orthopedics, 2008, 133, 30–37.
21. PAUWELS, R., O. NACKAERTS, N. BELLAICHE, H. STAMATAKIS, K. TSIKLAKIS, A.
WALKER, H. BOSMANS, R. BOGAERTS, R. JACOBS, K. HORNER, Variability of dental
cone beam CT grey values for density estimations, The British Journal of Radiology, 2013, 86,
20120135.
22. SCARFE, W.C., A.G. FARMAN, P. SUKOVIC, Clinical applications of cone-beam computed
tomography in dental practice, Journal of the Canadian Dental Association, 2006, 72, 75–80.
23. SHAPURIAN, T., P.D. DAMOULIS, G.M. REISER, T.J. GRIFFIN, W.M. RAND, Quantitative
evaluation of bone density using the Hounsfield index. The International Journal of Oral &
Maxillofacial Implants, 2006, 21, 290–297.
24. TURKYILMAZ, I., T.F. TOZUM, C. TUMER, Bone density assessments of oral implant sites
using computerized tomography, Journal of Oral Rehabilitation, 2007, 34, 267–272.

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